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INVITED REVIEW

Cybium 2000, 24(4): 319-342.

THE BRANCHIAL BASKET IN TELEOST FEEDING

by

Pierre VANDEWALLE (1), Éric PARMENTIER (1) & Michel CHARDON (1)

ABSTRACT.!-!In teleosts, feeding is effected principally by suction and food is handled by the branchialbasket. Preys are carried to the oesophagus by the pharyngeal jaws (PJs). The pharyngobranchial bonesconstitute the upper pharyngeal jaws (UPJs) and the 5th ceratobranchial bones, the lower pharyngeal jaws(LPJs). In lower teleosts, these jaws have well-separated spindly parts attached to the neurocranium,pectoral girdle, and hyoid bar; they only transport food and LPJ activity predominates. In acanthoptery-gians, the PJs become stronger, the left and right ceratobranchials fuse into one LPJ, and the pharyngo-branchials join together to form two big UPJs articulating with the neurocranium. In labrids and scarids,the LPJ is also joined to the pectoral girdle. In acanthopterygians, a new retractor dorsalis muscle givesthe UPJs the major role in food chewing and transport. Cypriniforms have developed original PJs withstrong 5th ceratobranchials opposed to a postero-ventral neurocranial plate. Small-sized preys and foodparticles are seized by the gill rakers, small skeletal pieces supported by the branchial arches.

RÉSUMÉ.!-!Le rôle de la corbeille branchiale dans l’alimentation des téléostéens.La prise de nourriture des téléostéens est surtout réalisée par aspiration et le traitement des ali-

ments est assuré par la corbeille branchiale. Les grosses proies sont amenées à l’œsophage par les mâchoi-res pharyngiennes. Les pharyngobranchiaux constituent les mâchoires supérieures et les cinquièmescératobranchiaux les inférieures. Chez les téléostéens primitifs, ces mâchoires sont grêles et forméesd’éléments osseux bien séparés, suspendus entre le neurocrâne, la ceinture scapulaire et la barre hyoï-dienne; elles n’assurent que le transport de la nourriture et le rôle des mâchoires inférieures est prédomi-nant. Chez les Acanthoptérygiens, les mâchoires pharyngiennes deviennent plus fortes, les cératobran-chiaux gauche et droit fusionnent en une mâchoire pharyngienne inférieure unique tandis que les pharyn-gobranchiaux se solidarisent pour constituer des mâchoires supérieures puissantes articulées au neuro-crâne. Enfin chez les Labridae et les Scaridae, la mâchoire pharyngienne inférieure est en plus articuléesur la ceinture scapulaire. Chez les Acanthoptérygiens, l’apparition d’un muscle rétracteur dorsal donneaux mâchoires supérieures le rôle principal dans le traitement et le transport de la nourriture. Les Cyprini-formes ont développé des mâchoires pharyngiennes originales constituées des cinquièmes cératobran-chiaux très puissants opposés à une plaque ventro-postérieure du neurocrâne. Les aliments de très petitestailles sont saisis par les branchiospines, petits éléments squelettiques portés par les arcs branchiaux.

Key!words.!- Teleosts - Branchial basket - Pharyngeal jaws - Gill rakers - Feeding.

In teleosts, suction feeding is the mechanism most commonly used to bring food intothe buccal cavity (Lauder, 1983a). Suction involves a succession of movements of the differ-ent head components, creating a backward-moving water stream (Osse, 1969; Vandewalle andChardon, 1981; Lauder, 1983a).

All fishes can perform suction, which is necessary to breathing (see for exampleBallintijn, 1969). Breathing movements are small, however, and prey capture requires fast,ample movements. In many cases, the buccal jaws have no contact with the food.

(1)!Université de Liège, Institut de Chimie, Laboratoire de Morphologie fonctionnelle et évolutive, Bâti-ment B6, Sart Tilman, B-4000 Liège, BELGIUM. [[email protected]]

320 VANDEWALLE ET AL.

Between the buccal cavity and the oesophagus, the branchial basket is believed to playan important role in food chewing, processing, and transport.

The aim of the present simplified synthesis is to present the morphology, movements,and biological roles of the elements of the branchial basket during feeding, with emphasis onthe pharyngeal jaws and gill rakers.

OSTEOLOGY

Pharyngeal jawsIn teleosts, the skeleton of the branchial basket consists of five branchial arches

(Fig.!1). The first three arches are complete, with a median basibranchial and, on each side, aseries of bones: a hypobranchial, a ceratobranchial, an epibranchial and a pharyngobranchial.The fourth arch consists at least of paired ceratobranchials and epibranchials, and sometimesadditionally of pharyngobranchials and a basibranchial (Nelson, 1969; Rosen, 1974). Hypo-branchials are seldom present (Holstvoogd, 1965). The 5th ceratobranchials form the base ofthe lower pharyngeal jaws (LPJs), and the 2nd, 3rd and 4th pharyngobranchials (according tothe case), that of the upper pharyngeal jaws (UPJs). All endochondral elements may be cov-ered by or connected to toothed dermal plates. The inner concave faces of the epibranchialsand ceratobranchials, and often those of the hypobranchials, bear two rows of small inter-locking skeletal pieces, the gill rakers.

Lower teleostsIn elopomorphs, which are primitive teleosts, the branchial basket hangs from the neu-

rocranium by levatores muscles. The pharyngeal jaws (PJs) are small (Forey, 1973; Taverne,1974). The independent lower pharyngeal jaws (LPJs) each bear a series of small, independenttoothed plates. The latter are continued by toothed plates borne by the basibranchials andbasihyal. The ceratobranchials, hypobranchials, and ceratohyals also bear toothed plates. Tothis ventral toothed-plate array is opposed a dorsal one. Posteriorly, the almost independentpharyngobranchials associated with toothed plates constitute the upper pharyngeal jaws(UPJs). In front of them, the parasphenoid and vomers bear toothed plates (opposite those ofthe basibranchials and basihyal). Laterally there are also teeth on the palatines, ectopterygoids,and entopterygoids. This means that in elopomorphs, the whole buccopharyngeal cavity fromthe mouth to the oesophagus is a large toothed system in which the PJs are not prominent. Allteeth are simple and sharp.

In the course of evolution, the number of toothed bones appears to have decreasedwhile the PJs became increasingly important. In osteoglossomorphs (Nelson, 1968;Greenwood, 1973; Taverne, 1977, 1978), the organisation of the branchial skeleton is muchlike that of elopomorphs (Fig.!1). The fifth ceratobranchials associated with the ventraltoothed plates of the LPJs are opposed to the dorsal toothed plates, the first of which consti-tutes with the pharyngobranchials the UPJs. The teeth are pointed and still numerous, despitetheir absence on the ceratohyals, epihyals, ceratobranchials, and epibranchials; the mediandorsal and ventral dentition is particularly developed (Taverne, 1977; Lauder and Liem,1983). Samford and Lauder (1989) even view osteoglossomorphs as possessing three succes-sive jaws: the buccal jaws, the parasphenoid-basihyal toothed apparatus, and the PJs.

The protacanthopterygians or lower Euteleostei include families such as the salmonidsand esocids (Greenwood et al., 1966). Their PJs are much like those of the osteoglossomorphsor elopomorphs, but their dentition is reduced in the buccal cavity and on the branchial arches(especially on the basibranchials) (Norden, 1961; Rosen, 1974; Weitzman, 1974). The

The branchial basket in teleost feeding 321

Fig.!1.!-!Dorsal view of the hyoid and branchial skeleton of Notopterus notopterus (adapted from Taverne,1978). The left branchiospines and tooth plates are removed. BB: basibranchial; BBT: basibranchial toothplate; BH: basihyal; CB: ceratobranchial; CH: ceratohyal; EB: epibranchial; EBT: epibranchial toothplate; EH: epihyal; GR: gill rakers; GT: gular teeth; HB: hypobranchial; HH: hypohyal; PB: pharyngo-branchial; PBT: tooth plate of the pharynobranchial; TBB: tooth plate of the basibranchials; TCB: toothplates of the ceratobranchial elements; TPB: tooth plates of the pharyngobranchial elements.

pharyngeal dermal toothed plates are often fused with the endochondral branchial elements(Rosen, 1974; Weitzman, 1974; Lauder and Liem, 1983). This reinforces the cohesion of thePJs, although the pharyngobranchials are but loosely bound together.


Fig.!2.!-!A: Ventral view of the upper pharyngeal jaw of Tilapia tholloni (adapted from Goedel, 1974);B:!Dorsal view of the lower pharyngeal jaw of Tilapia louka (adapted from Thys Van den Audenaerde,1970). CBT: ceratobranchial tooth plate; PB: pharyngobranchial; PBT: pharyngobranchial tooth plate.

Higher teleostsIn acanthopterygians, which possess a protrusive mouth (Greenwood et al., 1966), we

observe greater development of the PJs and the disappearance of teeth in the buccal cavity.Primitive acanthopterygians such as the centrarchids, haemulids, and serranids show

few to no teeth on the parasphenoid, vomer, entoglossal, and basihyal, and above all thereremain only a few teeth on the pterygoid bones (Benmouna et al., 1984a; Comes et al., 1988;Johnson and Fritzsche, 1989). The left and right LPJs are fused with their toothed plates, butremain free with respect to each other; they are attached to the rest of the branchial basket bytheir anterior ends. The UPJs consist of the second and third pharyngobranchials, each bearinga toothed plate, and of one posterior toothed plate (Liem, 1970; Rosen, 1973; Vandewalle etal., 1992). The three latter bones can be associated with toothed plates borne by the secondand/or third pharyngobranchials (Dineen and Stokely, 1956; Rosen, 1973; Wainwright,1989a). The discrete elements of this functional ensemble are but loosely bound together andhang from the skull by the first pharyngobranchial and the levatores muscles. The teeth aresharp and uni- or bicuspid. They differ in size according to the skeletal element, being muchsmaller on the posterior toothed plate than on the pharyngobranchials (Lauder and Liem,1983; Vandewalle et al., 1992).

In more specialised acanthopterygians such as the cichlids and embiotocids, there areno longer any teeth in the buccal cavity (Vandewalle, 1972; Liem and Osse, 1975; Liem,1978). The left and right LPJs are fused into a large triangular toothed plate (Nelson, 1967;Thys van den Audenaerde, 1970; Liem, 1973; Barel et al., 1977; Witte and Van Oijen, 1990)(Fig.!2). This single LPJ is opposed to paired UPJs. In cichlids, each UPJ consists of a small,toothed second pharyngobranchial and a large ensemble formed by the third and fourthpharyngobranchials. [Note that Liem (1978) describes a fourth pharyngobranchial in cichlids,while Lauder and Liem (1983) describe a posterior toothed plate in its place]. In embiotocids,the UPJs consist of only the third and fourth pharyngobranchials (Nelson, 1967a; Liem, 1986).

The UPJs of cichlids and embiotocids articulate with a posterior ventral apophysis ofthe parasphenoid through their third pharyngobranchials. Their teeth are often specialised


(unicuspid, bicuspid, tricuspid, molar-like, and so on) and adapted to the diet: microphagousand planctivorous species generally have small, crowded teeth while molluscivorous specieshave large, rounded teeth for crushing shells (Witte and Van Oijen, 1990). The size of the PJbones is also related to the diet. They are more slender in piscivorous than in molluscivorouscichlids (Hoogerhoud and Barel, 1978).

In labrids and scarids, the fifth ceratobranchials are fused into an often-large singleLPJ articulating posteriorly with the cleithra via a synovial joint (Quignard, 1962; Liem andGreenwood, 1981; Gobalet, 1989; Monod et al., 1994; Bullock and Monod, 1997). The UPJsconsist of large pharyngobranchials (Monod, 1951; Nelson, 1967a). They articulate through adiarthrosis with the pharyngeal process of the parasphenoid (Kaufman and Liem, 1982; Liemand Sanderson, 1986). The teeth can be specialised as in cichlids (Yamakoa, 1978).

Hemiramphids (Aterinomorpha) have also developed strong PJs, and notably a singletoothed LPJ articulating with the pectoral girdle opposite the distinct 2nd and large 3rdpharyngobranchials (Rosen and Parenti, 1981; Vandewalle, in prep.).

OstariophysiA parallel evolution is observed in the Ostariophysi. In characiforms, the mouth, usu-

ally not protrusive, bears many teeth, including palatial teeth (Bertin, 1958a; Roberts, 1969).The PJs are constituted by independent fifth ceratobranchials bearing toothed plates, facingtoothed pharyngobranchials loosely bound to one another (Weitzman, 1962; Roberts, 1969;Miquelarena and Aramburu, 1983). The branchial basket hangs under the neurocranium(Weitzman, 1962; Roberts, 1966). The teeth are conical and differ in size and number.

In catfishes, all the pharyngobranchials present contribute to the UPJs, except for thefirst ones. As in characiforms, they are loosely bound to one another (Mahy, 1974; Arratia,1987; Adriaens and Verraes, 1998).

Cyprinids have evolved a special protrusion mechanism (Ballintijn et al., 1972;Vandewalle, 1978), different from that of the acanthopterygians. The buccal jaws are com-pletely toothless (Ramaswami, 1955a, 1955b; Vandewalle, 1975). Teeth are borne only by thewell-developed fifth pharyngobranchials (PJs), which alone constitute the left and right PJs(Fig.!3). These PJs are associated with a chewing pad borne by the basioccipital (Ramaswami,1955a, 1955b; Sibbing, 1982) and acting as a UPJ (Fig.!3). The pharyngobranchials are thusexcluded form the PJs. Teeth are rare, often sharp and strong, but sometimes molariform(Ramaswami, 1955a, 1955b; Vandewalle, 1975; Sibbing, 1982).

Gill rakersGill raker (branchiospine) morphology (Fig.!1) is related to diet and can vary not only

from one species to another but even from one branchial arch to another within a species(Bertin, 1958b; Roberts, 1969; Whitehead and Teugels, 1985).

The hypo-, cerato- and epibranchials of elopomorphs bear rows of branchiospines, de-creasing in size from the outside to the inside. Most of them are denticulate.

In osteoglossomorphs, the branchiospines are very similar in morphology and disposi-tion to those of elopomorphs. There are just two rows of branchiospines per arch, except onthe fifth arch, where there is only one row (Fig.!1) (Taverne, 1977, 1978).

In clupeomorphs, gill raker organisation is very complicated (Kirchoff, 1958; Monod,1961). The gill rakers are often long and crowded, particularly on the ceratobranchials. On theepibranchials they may be transformed, forming part of a suprabranchial organ (Monod,1961). In Sierrathrissa leonensis for example, no ceratobranchial or epibranchial bears morethan 9 of them (Whitehead and Teugels, 1985).


Fig.!3.!-!Schematic lateral views of the neurocranium and pharyngeal jaws of Esocidae (modified fromLauder, 1983b), Haemulidae (modified from Wainwright, 1989a), Cichlidae and Labridae (modified fromLiem and Greenwood, 1981), and Cyprinidae (modified from Sibbing, 1982). AD!5: adductor 5 muscle;GH: geniohyoideus muscle; HB: hyoid bar; LEXT: elevator externus muscle; LP: levator posterior mus-cle; LPJ: lower pharyngeal jaw; NCR: neurocranium; OP: obliquus posterior muscle; PE: pharyngohyoi-deus externus muscle; PI: pharyngohyoideus internus muscle; RC: rectus communis muscle; RD: retractordorsalis muscle; RP: retractor posterior muscle; SC: scapular girdle; STH: sternohyoideus muscle;UPJ:!upper pharyngeal jaw.


In salmonids, the branchiospines show considerable variation (Berg, 1948; Scott andCrossman, 1973). They are more numerous and longer in planktivorous species (e.g., Core-gonus alba) than in euryphagous ones (e.g., Salmo trutta). They generally bear denticles, thenumber and size of which are related to the diet (Hessen et al., 1988).

In acanthopterygians the gill rakers also vary considerably. Only some examples arepresented here. In some serranid species, the gill rakers are denticulate; their length decreasesfrom the first to the fourth arch and they are larger on the outer than on the inner side (Ben-mouna et al., 1984a).

In mugilids, the general organisation of the gill rakers is quite constant, but original.The angle between the inner and outer gill raker rows varies from 45° to 180°. Each gill rakerbears two rows of secondary gill raker processes, which are conical, cylindrical, or flattened.On certain arches, the secondary processes in turn bear tertiary expansions constituted byprojections of epithelial cells (Guinea and Fernandez, 1992).

In cichlids, the branchiospines are simple or bear a single toothed plate (Vandewalle,1971, 1972). Moreover, there is a serried row of microbranchiospines on the lateral (external)sides of the 2nd, 3rd, and 4th branchial arches (Greenwood, 1953; Gosse, 1956; Beveridge etal., 1988).

Microbranchiospine-like structures have also been found in several other percoids(Greenwood, 1976; Stiassny, 1981).

The generally simple branchiospines of the ostariophysans vary only in size and num-ber (Weitzman, 1962; Gauba, 1969; Lammens and Hoogenboezem, 1991). In characins, how-ever, they are sometimes shaped like small, toothed balls (Roberts, 1969), and in some speciesthere is only one row per arch (Roberts, 1966; Miquelarena and Aramburu, 1983).

In gonorynchiforms, considered to be closely akin to the Ostariophysi (Rosen andGreenwood, 1970; Nelson, 1994), the branchiospines are simple, but those of the last twoarches contribute to supporting a suprabranchial organ quite similar to that of clupeids(Monod, 1949, 1963; Thys van den Audenaerde, 1961).

MUSCULATURE

Pharyngeal jawsGenerally speaking, the muscles related to the PJs vary little among teleosts. Some

differences, however, have a major functional impact, making it necessary to consider twotypes of branchial musculature: that of lower teleosts and that of acanthopterygians. The list ofbranchial muscles presented below for the lower teleosts is based on a survey of the literature(Vetter, 1878; Dietz, 1912; Holstvoogd, 1965; Bishai, 1967; Nelson, 1967b; Greenwood,1971; Winterbottom, 1974; Lauder and Liem, 1980; Lauder, 1983b).

Lower teleostsThere are four levatores externi inserting at one end on an epibranchial and at the

other end on the neurocranium. There are two to three levatores interni extending from thesecond and third pharyngobranchials to the neurocranium. In most cases, these muscles lift theUPJs and shift them forward at the same time. In esocids, however, at least the first two leva-tores muscles draw the UPJs backward (Holstvoogd, 1965; Lauder, 1983b). Generally thelevatores externi, the upper insertion of which is more external than the lower one, adduct theleft and right UPJs. Two transversi dorsales, binding two left epibranchials to their right sym-metricals, draw them together.


There can be an adductor between the ceratobranchial and the epibranchial of a samearch. The fifth adductor, always present, binds the fourth epibranchial to the fifth ceratobran-chial. It lifts the posterior part of one LPJ (left or right).

The LPJs are adducted by two transversi ventrales extending between the left and rightfourth and fifth ceratobranchials. Usually, the rectus communis joins the fifth ceratobanchialto the third hypobranchial, but interspecies variation is observed (Dietz, 1912; Nelson, 1969;Greenwood, 1971; Winterbottom, 1974). The main role of the rectus communis is to lower theLPJ. Sometimes recti ventrales join one ceratobranchial to the preceding hypobranchial.

The pharyngocleithrales interni and externi extend from the pectoral girdle to theLPJs. The pharyngocleithrales interni draw the PJs backward and the pharyngocleithralesexterni draw them downward. At the same time these muscles pull the PJs apart.

It seems that the obliqui ventrales joining the first hypobranchials and ceratobranchialsexert little influence on the PJs.

The sternohyoideus extending from the urohyal to the pectoral girdle may pull thehyobranchial system backward, while the geniohyoidei joining the lower jaw with the hyoidbars may pull this system forward.

In summary, the PJs are lifted by the levatores muscles, lowered by the pharyngoclei-thralis externus and rectus communis, pulled forward by the geniohyoideus and levatores, andpulled backward by some levatores, the pharyngocleithralis internus, and the sternohyoideus.They are brought together by the adductores and pulled apart by the simultaneous activity ofthe levatores and the pharyngocleithralis externus. The observed complex movements of thePJs depend on the ordered contraction of many branchial muscles.

Higher teleostsThe branchial musculature of acanthopterygians differs from that of the lower teleosts

by the following features (Liem, 1970, 1973, 1978, 1986; Vandewalle, 1972; Yamakoa, 1978,1980; Lauder, 1983a, 1983b; Benmouna et al., 1984b; Vandewalle et al., 1992) (Fig.!3). Allthe levatores externi and interni are turned forward; they lift, protract, and pull apart the UPJs.The fourth levator externus is more developed than the others. Part of it may be fused withpart of the obliquus posterior (which joins the fifth ceratobranchial with the fourth epibran-chial and thus works as a levator of the fifth ceratobranchial (Aerts, 1982; Liem, 1986; Gallis,1993, 1994).

A levator posterior extends from the back of the skull to the fourth epibranchial and,thanks to this nearly vertical orientation, works as a perfect levator (Fig.!3). Like the fourthlevator externus, it is sometimes fused with part of the obliquus posterior and thus also be-comes a levator of the fifth ceratobranchial (Claeys and Aerts, 1984; Liem, 1986). Such isnotably the case in labrids, where this muscle is often so highly developed that it inserts at thetop of the skull (Yamaoka, 1978).

A big retractor posterior extends from at least the third pharyngobranchial to the ven-tral surface of the first vertebrae. It lifts and pulls each UPJ backward (Fig.!3). The existenceof this muscle seems related to the forward orientation of all the levatores externi.

Last of all, the pharyngohyoideus (homologous to the rectus communis, according toLauder (1983b), extends from the fifth ceratobranchial to the urohyal; the length of its fibresand the mobility of the urohyal increase the possibilities of movement of the LPJs (lowering,pulling apart the left and right parts, and even forward displacement).

Wainwright (1989b) reports that in some acanthopterygians such as the haemulids, theprotractopectoralis muscle inserts on the neurocranium and on the fifth ceratobranchial, not onthe pectoral girdle; it thus occupies the place of a levator posterior.


Fig.!4.!-!A: Lateral side of the gill arch; B: Medial side of the gill arch (adapted from Hoogenboezem etal., 1991). ABS: abductor branchiospinalis muscle; CB: ceratobranchial bone; CN:!channel; CT: compactconnective tissue; CU: raker cushion; GR: gill raker; IB: interbranchiospinalis muscle; IBS: constrictorcanalis interbranchiospinalis muscle; LR: lateral gill raker; RA: raker articulation.

Despite a general plan common to all teleosts, the acanthopterygians possess somespecial muscles, the size of which suggests a more important role of the PJs in food handling.Among the upper teleosts, furthermore, the development of the pharyngeal muscles is relatedto diet. A fish-eating cichlid, for example, has far less bulky branchial muscles than a mollus-civorous one (Hoogerhoud and Barel, 1978).

In hemiramphids, the branchial musculature differs from that of the acanthopterygiansonly by a retractor dorsalis of the 2nd pharyngobranchials, inserting at the back of the neuro-cranium (Vandewalle et al., in prep.).


OstariophysiIn Ostariophysi, the particularities of the branchial skeleton are associated with an

original musculature. The branchial muscles of characiforms are much like those of the lowerteleosts (Gijsen and Chardon, 1976). Cypriniforms, on the contrary, with their powerful PJconstituted only by the fifth ceratobranchials, have evolved an original musculature (Takahasi,1925; Holstvoogd, 1965; Winterbottom, 1974; Vandewalle, 1975; Sibbing, 1982) (Fig.!3).There is an enormous retractor posterior ensemble between the PJs and the posterior processof the basioccipital, and a bulky levator branchialis 5 between the PJ and the neurocranium.Ventrally, there is a large transversus muscle, the contraction of which brings the PJs towardeach other and at the same time rotates them axially so that the teeth are properly turned to-ward the skull (Sibbing, 1982).

Gill rakersThere are muscles associated with the gill rakers, despite past partial confusion with

the branchial filament muscles (Bijtel, 1949; Hoogenboezem et al., 1991). Descriptions arerare and the most thorough studies concern cyprinids (Hoogenboezem et al., 1991; Van denBerg et al., 1994a). Despite discrepancies between the two cited papers, we may consider foreach gill raker the following muscles (Fig.!4):

-!The adductor branchiospinalis is a thin sheet of fibres inserting on the side of eachexternal gill raker (Hoogenboezem et al., 1991) and, at the other end, on the base of the cor-responding branchial filament (Van den Berg et al., 1994a). There is no such muscle on theinternal branchiospines; it would seem to be only partly distinct from the abductor filamenti.The abductor branchialis lowers the gill raker.

-!The interbranchiospinalis, inserting via tendons on two successive external gill ra-kers, is described by Hoogenboezem et al. (1991) in 30-cm Abramis brama specimens, butVan den Berg et al. (1994a) failed to find it in two 14.9-cm (SL) Blicca bjoerkna specimens,Rutilus rutilus, and Abramis brama. This muscle may control the distance between successiveexternal gill rakers.

-!The constrictor canalis interbranchiospinalis is very complex morphologically(Hoogenboezem et al., 1991; Van den Berg et al., 1994a). It extends from the ventral side ofthe ceratobranchial to the bottom of a channel and up inside the walls of the same channel(Hoogenboezem et al., 1991). According to Van den Berg et al. (1994a), its functions mightbe (a) to act as an abductor branchiospinalis, (b) to contract the soft tissues of the branchiospi-nes so as to squeeze out the mucus from the caliciform cells, and (c) to straighten the chan-nels.

MOVEMENTS AND FUNCTIONS

Among the branchial basket structures, the PJs are particularly related to a macro-phagous diet, while the branchiospines are essential to a microphagous diet. In a same speciesthe diet usually changes during growth and a same food item may be macroscopic for the fryand microscopic for the adult fish. Monophagous teleosts are few, and the diet often changesaccording to the season and to food availability (Boikova, 1986).

Cineradiographic and electromyographic techniques are required to observe PJmovements. Such observations are extremely difficult because of the deep positions of thevery thin muscles embedded in the very delicate and highly vascularised branchial lamellae.

As it is generally assumed that the PJs play a greater role in food handling in higher


than in lower teleosts, this role has been studied more frequently in the former, and neglectedin the latter.

Pharyngeal jawsLower teleostsLauder (1982, 1983b) divides food capture in Esox niger into four distinct phases: ini-

tial strike, buccal manipulation, pharyngeal manipulation, pharyngeal transport (includingdeglutition). During the initial strike, some muscles (third and fourth levatores, fifth adduc-tor,!…) work variably, in a manner suggestive of a preparatory phase and a positioning of thePJs. During the two manipulation phases, the third and fourth levatores and the pharyngoclei-thrales exerni and interni are active, while the fifth adductor is no longer working. As a result,the lower and upper pharyngeal jaws move apart, especially in front, as for a forward-orientedgape. These movements probably allow a good orientation of the prey relative to the PJs,ready to seize it, before pharyngeal transport.

The three periods just described are brief and devoid of cyclic events. Pharyngealtransport, on the contrary, lasts long (several minutes) and comprises repeated and rathersimilar cycles of muscle activity; it is the most important phase in food capture in Esox.

During transport, the sternohyoideus does not work, and the geniohyoideus andpharyngocleithralis are but occasionally active. The first and second levatores externi worksimultaneously with the pharyngocleithralis externus, so that the upper and lower pharyngealjaws are pulled backward at the same time (or nearly so). The third and fourth levatores ex-terni are the antagonists of the former muscles, and protract the UPJ. However, taking intoaccount the orientation of the levatores externi, these longitudinal movements of the UPJ seemlimited. In Elops saurus, only the first levator is not inclined forward (Winterbottom, 1974),while in Salvelinus fontinalis, all the levatores are inclined backward (Lauder and Liem,1980). It thus seems that the backward displacements of the PJs are passive (Lauder, 1983b).

The only variability observed in Esox muscle activity is a possible asymmetry in theactivities of the third and fourth left and right levatores (Lauder, 1983b).

According to Lauder (1983b), the UPJs and LPJs of Esox move together backward andto the midline, then forward and sideward, but the longitudinal movements of the LPJs may begreater, as suggested by the muscles. The movements predominating in food transport seem tobe those of the LPJs, and anatomical observations suggest the same for other lower teleosts(Lauder, 1983b). Prey progression results from the difference in amplitude of the longitudinalmovements of the upper and lower pharyngeal jaws. The PJs simply transport the prey to theoesophagus, without crushing or otherwise transforming it.

In the osteoglossomorph Notopterus chitala, intermediate jaws (parasphenoid andbasihyal) seem to initiate transport the prey to the oesophagus (Sanford and Lauder 1989,1990); the PJs are probably associated with them. The parasphenoid, attached to the neurocra-nium, may merely hold the prey fast while the basihyals transport it by means of broad longi-tudinal displacements. It is thus probable that the LPJs, placed just behind the basihyals, playthe main role in prey transport, as in Esox.

Higher teleostsLauder (1983b) considers the same four phases in food capture in primitive acantho-

pterygians as in Esox, but Wainwright (1989a) believes there is no pharyngeal manipulation inhaemulids and that in 90% of cases only seizing and transport are present. Food would thus bebrought directly to the PJs.

Pharyngeal muscle activities are recorded during the first phases of prey capture. Theyare probably needed to place the PJs in the right position for seizing the prey.


Fig.!5.!-!Summary “block diagram” of muscle activity during pharyngeal transport in Lepomis microchi-rus. The left and right edges of the bars mark the mean time of onset and offset of muscle activity and thethin line indicates one standard error of this mean (adapted from Lauder, 1983c). Black bars indicateactivity in 67-100% of all experiments, shaded bars indicate activity in 34-66% of them, and white barsindicate activity in 1-33% of them. AD!5: adductor branchialis 5 muscle; LEXT 1,!2: levatores externimuscles 1,!2; LEXT 3,!4: levatores externi muscles 3,!4; LP: levator posterior muscle; PE: pharyngoclei-thralis externus muscle; PI: pharyngocleithralis internus muscle; RC: rectus communis muscle;RD:!retractor dorsalis muscle.

During the transport phase, rather regular periodic activities of the branchial musclesare observed. The retractor dorsalis is particularly active (Fig.!5), while the sternohyoideus isoften silent (Lauder, 1983b, 1983c; Wainwright, 1989a, 1989b).

A characteristic broad overlapping of the periods of activity of most muscles (Lauder,1983b, 1983c; Wainwright, 1989a, 1989b) means that the movements of the upper and lowerpharyngeal jaws are neither simultaneous nor in phase opposition, but simply asynchronouswith the same frequency. The PJs thus do not move in opposite directions during part of thecycle. The UPJs are lifted (by the levator posterior and the third and fourth levatores externi),then pulled backward (by the retractor dorsalis), while the LPJs are retracted (by the pharyn-gocleithralis internus). Then the UPJs and LPJs are adducted (by the fifth adductor), but theLPJs are pulled forward (by the pharyngohyoideus and maybe by the geniohyoideus) whilethe UPJs are always shifted backward (by the retractor dorsalis). At the end of the cycle theLPJs are lowered (by the pharyngocleithralis externus) while the UPJs are protracted either bythe first and second levatores externi or probably, in part, by inertia (Lauder, 1983b, 1983c).Before a new cycle begins, the PJs are actively repositioned (by the first and second levatoresexterni, the pharyngocleithralis externus and pharyngohyoideus) to their former anterior place,apart from each other (Lauder, 1983c). Contrary to observations on Esox, the UPJs play thepredominant role in transporting food (Lauder, 1983b).

Lauder (1983b, 1983c) and Wainwright (1989b) think that, despite some asymmetriesin the activities of the first and second levatores externi, the pattern of food transport is ratherconstant whatever the sort of prey (except in snail-crushing Lepomis microlophus). Vande-walle et al. (1992), on the contrary, observed major modulations of food transport movementsin Serranus scriba. In this species, the movements of the PJs for transporting food into theoesophagus are either in phase opposition or asynchronous or simultaneous (Fig.!6).


Fig.!6.!-!A: Graphic representation of the antero-posterior movements of the left pharyngeal jaws ofSerranus scriba; B: Displacement of a prey (a small fish, Xiphophorus maculatus) (adapted from Vande-walle et al., 1992b). The maximum error on displacements is 0.4. The arrows indicate prey capture andswallowing. The vertical lines delimit the six successive anteroposterior movements of the left UPJ duringprey transport. A: anterior; P: posterior.

In most cases, the cycles of the UPJs have a greater amplitude than those of the LPJs,a fact also observed by Lauder (1983b) in the centrarchid Micropterus salmoides. The effi-ciency of the transport movements is variable: transport is faster if the movements of the PJsare in phase opposition, especially if the prey is protected by hard teguments. Transport is alsopossible when the left and right UPJs move in opposite directions or with different amplitudes,or even when only one UPJ is working (Vandewalle et al., 1992). Such different movementpatterns imply equally different muscle activity patterns.

Vandewalle et al. (1992) further report that the three skeletal elements of the UPJs ofSerranus scriba retain some reciprocal freedom, so that their displacements are not alwaysidentical and their reciprocal orientations are somewhat variable. The general shape of theUPJs is thus variable, showing an upward or a downward curvature, probably in response to


Fig.!7.!-!Diagrammatic lateral view of pharyngeal jaw orbits derived from measurements obtained fromcineradiographic film sequences of the labrid Tautoga onitis during mastication and swallowing. Theanterior end is to the left. The orbits drawn indicate the motion of a point on the posteroventral corner ofthe upper pharyngeal jaw. During mastication: 1: resting positions; 1-4: shearing (activity period of thelevator externus 4 and internus muscles); 4-5: transitional phase (activity period of the levator externus 4and levator posterior muscles); 5-6: crushing (activity period of the levator externus 4, levator posteriorand retractor dorsalis muscles); 6-1: recovery (activity period of the pharyngocleithrum externus muscle).During swallowing: 1-3: protraction; 3-4: retraction; 4-1: recovery. LPJ: lower pharyngeal jaw;UPJ:!upper pharyngeal jaw (adapted from Liem and Sanderson, 1986).

prey particularities and behaviour. Such possibilities for deformation are likely to be shared byall teleosts provided with well-separated and loosely connected PJ elements.

The PJs of primitive acanthopterygians, protacanthopterygians, and osteoglosso-morphs generally perform food transport only, through varied movements. All these possibili-ties of movement are related to the reciprocal freedom of the left and right, upper and lowerpharyngeal jaws, and to their independence with respect to the skull and pectoral girdle. Preysare swallowed whole, without traces of injury or mechanical trituration by the PJs. The cen-trarchid Lepomis microlophus seems to be an exception in this regard. Lauder (1983c) reportsthat this species can break the shells of certain snails between the PJs before bringing theminto the oesophagus, but other types of prey are just transported.

In higher acanthopterygians, the LPJs are fused together and the UPJs consist of verytightly bound elements articulating on the ventral surface of the skull. In cichlids, Liem(1978), Aerts et al. (1986), Claes and De Vree (1989, 1991), and Claes et al. (1991) describecyclic movements of the PJs during feeding, but these movements follow very different pat-terns according to the type of food. In Oreochromis niloticus, an earthworm, for example, istransported to the oesophagus by regular movements of the PJs (Claes and De Vree, 1991;Claes et al., 1991); the movements of the upper and lower pharyngeal jaws are in oppositedirections or nearly so, and they barely alter the shape and structure of the prey (Claes and DeVree, 1991). When the same species is fed hard pellets, major masticating movements areobserved. The pellets are crushed and sheared by opposite movements of the upper and lowerPJs before being swallowed (Aerts et al., 1986; Claes and De Vree, 1991). Gallis (1994),furthermore, shows flexible muscle activity patterns during crushing in response to changes indemand. Haplochromis (= Dimidiochromis) compressiceps chews small fish by in-phasemovements of the PJs (Liem, 1978). This seems to be an exception. In both Oreochromis


niloticus and Astatotilapia (= Haplochromis) burtoni, movements in phase opposition areinvolved in chewing the same sort of prey (Liem, 1986; Claes and De Vree, 1989). Cichla-soma minckleyi crushes mollusc shells by the same movements (Liem and Kaufman, 1984).Mastication may be performed preferentially by one UPJ and then by the opposite one (Claesand De Vree, 1989). Liem (1978) also reports activity periods of the pharyngeal musclessuggesting that the left and right UPJs are not always moved simultaneously. The amplitude ofthe handling cycles depends on the sort of prey, but the longitudinal movements of the UPJsare, as in lower acanthopterygians, more ample than those of the LPJs (Claes and De Vree,1991).

Liem (1986) describes regular chewing cycles in embiotocids, with particularly cons-tant muscular activity patterns whatever the food. The horizontal components of the move-ments of the upper and lower PJs are equal during chewing. Shearing and crushing result fromin-phase movements, but during swallowing, the horizontal movements of the LPJs are clearlysmaller than and somewhat in advance relative to those of the UPJs. This results in the back-ward displacement of the prey.

In cichlids and embiotocids there is thus pharyngeal reduction of food, distinct fromfood transport and swallowing. This is to be related to the partial fusion of at least the fourthlevator and/or the levator posterior with the obliquus posterior (Aerts, 1982; Claeys and Aerts,1984; Liem, 1986). These muscles transformed into levatores of the mandible, would allowmore power for pressing the prey between the PJs and consequently crushing it (Liem, 1978,1986; Liem and Kaufman, 1984).

In labrids and scarids, viewed as the most specialised teleosts (Liem and Greenwood,1981; Lauder and Liem, 1983b; Monod et al., 1994), the joint between the LPJ and the pecto-ral girdle causes stabilization of the LPJ, decreasing its freedom and causing its movements tobe influenced by those of the girdle. The LPJ becomes a lever (Liem and Greenwood, 1981)and the muscles moving it (such as the levator posterior; Yamaoka, 1978) may be highlydeveloped. The pharyngeal apparatus is a powerful crushing device, and movements of theneurocranium may contribute to crushing (Liem and Sanderson, 1986). Crushing cycles con-sist of “figure!8” movements with equal horizontal amplitudes for the lower and upper PJs(Fig.!7). The UPJ and LPJ are in phase when crushing or shearing. Characteristic large down-ward movements of the LPJ are observed (Liem, 1986). Swallowing movements are much likethose of embiotocids (Liem, 1986; Liem and Sanderson, 1986).

The main feeding strategy of acanthopterygians is to suck in preys and handle them atthe level of the PJs, but other feeding behaviours exist. For example, some cichlids crushmolluscs with the buccal jaws (Witte and Van Oijen, 1990) and several sparids crush hardpreys with their buccal jaws before transporting them to the oesophagus with the PJs (Vande-walle et al., 1995).

OstariophysiIn characiforms the branchial apparatus is much like that of lower teleosts, and it

seems to function similarly in prey catching (Lauder, 1983a). In cyprinids, food is manipu-lated by the PJs with the help of the posterior floor of the neurocranium. Chewing sequencescomprise trains of rhythmic cycles and end by swallowing movements. Sibbing (1982, 1991)divides each chewing cycle of Cyprinus carpio into three periods: a preparatory stroke, afeeding period called a power stroke, and a recovery stroke during which the skeletal elementsare positioned as at the beginning of the cycle. During the preparatory stroke, the jaws arebrought to a low position (principally by the pharyngocleithralis externus and rectus commu-nis) convenient for seizing food; at this time, the gap between the floor of the skull and thejaws is wide. The period of food manipulation consists of a crushing phase and a grinding


phase. During the crushing phase, the PJs are lifted (by the levator posterior, retractor poste-rior, and transversus ventralis) and pressed against the basioccipital, closing the entry of theoesophagus and squashing the food. In the grinding phase the PJ are pulled backward (mainlyand at least by the pharyngocleithralis internus, the retractor posterior, and the epaxial mus-culature), while the neurocranium rotates forward. In some chewing cycles crushing predomi-nates, in others, grinding. At the end, the reset phase brings the PJs forward again and theskull downward (by relaxation of most muscles and contraction of the pharyngocleithralisexternus). One or more chewing phases are followed by the swallowing stroke, during whichthe constrictor pharyngis and pharyngocleithralis externus show particular activity, whilecharacteristic constrictions of the posterior pharynx and low-amplitude chewing-like move-ments are observed (Sibbing et al., 1986).

In Cyprinus carpio, the PJ activity pattern varies according to the type of food. Notonly the number and frequency of cycles may vary, but also the identity of the muscles atwork. According to Sibbing (1982), the primary function of the pharyngeal apparatus is in-deed chewing, but other roles are important in food mixing, lubrication, and transport.

Gill rakersFilter feeding, (defined as feeding on prey of much smaller size than the predator

(Weihs and Webb, 1983), relies on a backward water current in the buccal cavity. The currentis induced by swimming while holding the mouth wide open and/or by active movements ofthe buccal and opercular pumps (Ballintijn, 1969; Vandewalle and Chardon, 1981) thatmodulate the filtration rate. In Brevoortia tyrannus, the swimming speed increases approxi-mately hyperbolically with increasing prey density (Durbin et al., 1981). When Engraulismordax feeds on Artemia nauplii, it alternates two- to three-second active swimming periodsduring which the mouth is open with brief, passive glides during which the mouth is closed(Leong and O’Connel, 1969). Many filter-feeder cyprinids, on the contrary, swim slowly ornot at all during filtration, which results from powerful ventilation-like movements (Sibbing,1991).

The highly variable number and shape of gill rakers in teleosts are related to the diet(Zander, 1906; Bertin, 1958b; Kirchhoff, 1958; Mathes, 1963). Hyatt (1979) reports that thebranchial sieve of benthic feeders is generally made of short gill rakers, while the gill rakers ofzooplanktivorous fishes are long. For example, the branchiospines of Crenicichla multispi-nosa and Abramis brama (Vandewalle, 1971; Hoogenboezem et al., 1991) are shorter thanthose of Clupea harengus (Kirchhoff, 1958). Lammens (1985), however, shows that thebream, Abramis brama, easily traps zooplankton.

It is generally believed that the size of the preys or particles trapped is related to thesize of the sieve mesh. Fish with smaller interraker distances are expected to be able to trapsmaller items (Gibson, 1988). Durbin and Durbin (1975) observed in Brevoortia tyrannus thatthe size of most preys caught was equal to or larger than the mean pore size of the sieve(80!µm), but two percent of the preys were clearly smaller.

According to King and McLeod (1976), the branchial sieve mesh is the interval be-tween gill rakers on each arch. This view is not in complete agreement with thetwo-dimensional interarch slit model (Zander, 1906), also called interdigitation model (Sib-bing, 1991). In the latter, widely accepted model (for example Greenwood, 1953; Matthes,1963), the measure of the mesh is the distance between a gill raker of the lateral row of onearch and the opposite one of the mesial row of the following arch. The interarch slit modelrests functionally on the ability to modulate the breadth of the branchial slits according to thesize of potential preys. In some species, the filtering efficiency is improved by microbranchio-spines that can trap much smaller items (Greenwoood, 1953; Gosse, 1956).


Fig.!8.!-!The “channel model”, food particles are presumably retained in a channel formed by two adjacentgill rakers. CN: channel; GA: gill arch; GR: gill raker; LGR: lateral gill raker; MGR: mesial gill raker(adapted from Hoogenboesem et al., 1991).

The interdigitation model, however, does not explain satisfactorily why the breamcaptures preys smaller than the interarch slit. This is why Hoogenboezem et al. (1991) haveproposed the “channel model” (Fig.!8). Each gill arch displays transverse ridges, each con-sisting of a cushion-like structure and a bony distal end. The space between two adjacentridges forms a channel with a rounded bottom. The extremity of each lateral gill raker canmove individually and can enter the mesial channel facing it on the next arch, and vice versa.With this structural ensemble are associated muscles (see above) that can straighten the chan-nels and shift the lateral gill rakers down and laterally. The mobility of the gill rakers and thefact that the arches can be brought closer together might explain, notably, how the bream trapssmaller particles, perhaps choosing food items individually. This interpretation gives no roleto mucus in food retention.

According to Van den Berg et al. (1994b), the model would apply only to facultativefilter-feeders that filter only small amounts of water, because it implies small-amplitudemovements of the branchial arches to modulate the mesh size. It should not apply to truefilter-feeding cyprinids possessing a very thin-meshed sieve, performing ample movements ofthe branchial arches, and filtering a large volume of water. For these, another model should beinvestigated. Van den Berg et al. (1994b) hypothesise that the particles trapped in the reducedchannels stimulate the mucous cells of the walls of the channel and are encapsulated in amucous layer, so that they stick to the wall and need no longer be retained by the lateral bran-chiospines. The mesh might also be reduced by the boundary layer created around the gillrakers as water is flowing through the sieve.

Sorting particles of food value is possible only if the gill rakers are particularly wellequipped with taste buds and able to react individually. In the case of cyprinids, the vo-mero-palatine organ (on the buccal roof) can sort and aggregate in mucus strands very small


food particles, such as diatoms, so that the branchial sieve can trap them (Sibbing and Uribe,1985).

To end this paragraph we will add more confusion to the debate by evoking the ex-periments of Drenner et al. (1987), showing that gill raker or microbranchiospine ablationdoes not modify at all the ability of cichlid Tilapia galilea (=!Sarotherodon galileus) to trapparticles when filter feeding.

CONCLUDING REMARKS

1.!Structural and functional comparisons of the branchial basket in teleosts revealbroad morphological diversity, albeit showing major evolutionary trends. From the Cretaceousperiod to the present, archaic teleosts such as the extant Elops saurus, whosebucco-pharyngeal dermal bones all bear teeth or toothed dermal plates, have coexisted withother teleost lineages showing various degrees of specialisation of the hyobranchial skeleton.The success of these taxa or lineages is very unequal, and one evolutionary trend has provedmuch more successful: the acanthopterygians, which became progressively dominant in ma-rine waters during the cenozoid and now predominate in African rift lakes. In acanthoptery-gians, the PJs appear to have improved in various ways, particularly with new articulations ofthe PJs on the skull and scapular girdle and concomitant muscle specialisations. The mostspecialized orders or families (Cichlidae, Embiotocidae, Labridae) are particularly rich inspecies. Liem and Osse (1975) attribute the incredible adaptative radiation of cichlids in Afri-can lakes to the separation of functions in handling food between the buccal and pharyngealjaws, allowing major adaptative transformations of both. The Ostariophysi are another groupthat has proven successful in fresh waters. Their main advantage could be the Weberian appa-ratus, more than any otherwise interesting but diverse transformations of the pharyngeal jaws,especially in cyprinids.

2.!In lower teleosts, the main movements enabling the transport of food from the buc-cal cavity to the oesophagus are those of the ventral part of the hyobranchial apparatus. A newmotor pattern appears in higher teleosts. A new muscle, the retractor dorsalis, gives the mainrole to the UPJs. In modern acanthopterygians, there are probably two motor patterns, one forfood transport and a second for food manipulation. Cyprinid fishes show an original mecha-nism, supported by a new organisation of the branchial basket skeleton and musculature.

3.!The notion “pharyngognathi” deserves discussion. The term was first used byMüller (1844) for a new taxonomic group including fishes whose pharyngeal bones are fusedat the midline. More recently, Bertin and Arambourg (1958) used “pharyngognath” as anadjective, and Liem and Greenwood (1981) describe “pharyngognathy” in many families ofhigher teleosts, among which “the monophyletic assemblage” of the Pomacentridae, Cichli-dae, Embiotocidae, and other Labroidei. These authors do not recognise pharyngognathy inthe Nandidae, which possess hyal and parasphenoid teeth. But what about the Serranidae andHemiramphidae? In fact, there is no morphological discontinuity in the food handling andtransport apparatus from lower acanthopterygians such as serranids to modern perciforms suchas scarids. This is why we propose to call “pharyngognathi”, on a functional basis, all teleostshandling and transporting food with the PJs. Such a clearly polyphyletic assemblage wouldcomprise the labrids, cichlids, serranids, maybe the lophiids… and also the cyprinids.

4.!All teleosts have gill rakers that play a role in filtering water, to protect the thin se-condary branchial lamellae and in some cases to catch small preys. Perhaps one should viewall teleosts as facultative filter-feeders (sensu Van den Berg et al., in press a). The branchio-spine sieve is liable, in any teleost lineage, to transform into a more efficient filtering sieve, by


complexification, lengthening of the gill rakers, or reduction of the interraker distance. Thevery mechanism of filter-feeding remains poorly understood. It seems to be different in diffe-rent species. In some cases, it seems to allow sorting of edible particles.

Acknowledgements.!-!The authors wish to thank K. Broman for improving the English of the manuscript.

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Reçu le 21.08.2000.Accepté pour publication le 30.11.2000.

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